Methotrexate cross-resistance in a mitoxantrone-selected multidrug- resistant MCF7 breast cancer cell line is attributable to enhanced energy- dependent drug efflux

Cancer Research

Volumn 60, Issue 13, 2000, Pages 3514-3521

  Volk, Erin L ^a,b   Rohde, Kristin ^a   Rhee, Myung ^a   McGuire, John J ^c   Doyle, L Austin ^d,e   Ross, Douglas D ^d,e,f   Schneider, Erasmus ^a,b  

^a WADSWORTH CENTER   (United States)

^b STATE UNIVERSITY OF NEW YORK   (United States)

^c ROSWELL PARK CANCER INSTITUTE   (United States)

^d UNIVERSITY OF MARYLAND   (United States)

^e UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^f BALTIMORE VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; METHOTREXATE; MITOXANTRONE;

ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CROSS RESISTANCE; DRUG UPTAKE; ENZYME ACTIVITY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MULTIDRUG RESISTANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY;

ANTINEOPLASTIC AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; BREAST NEOPLASMS; CELL SURVIVAL; DRUG RESISTANCE, MULTIPLE; FEMALE; HUMANS; METHOTREXATE; MITOXANTRONE; NEOPLASM PROTEINS; PEPTIDE SYNTHASES; RECOMBINANT PROTEINS; TRANSFECTION; TUMOR CELLS, CULTURED;

EID: 0034234294     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (58)

1. Moscow, J. A. Methotrexate transport and resistance. Leuk. Lymphoma, 30: 215-224, 1998.
2. Dixon, K. H., Lanpher, B. C., Chiu, J., Kelley, K., and Cowan, K. H. A novel cDNA restores reduced folate carrier activity and methotrexate sensitivity to transport deficient cells. J. Biol. Chem., 269: 17-20, 1994.
3. McGuire, J., Hsieh, P., Coward, J., and Bertino, J. Enzymatic synthesis of folylpolyglutamates. J. Biol. Chem., 255: 5776-5788, 1980.
4. Galivan, J. Transport and metabolism of methotrexate in normal and resistant cultured rat hepatoma cells. Cancer Res., 39: 735-743, 1979.
5. Jansen, G., Mauritz, R., Drori, S.. Sprecher, H., Kathmenn, I., Bunni, M., Priest, D., Noordhuis, P., Schornagel, J., Pinedo, H., Peters, G., and Assaraf, Y. A structurally altered human reduced folate carrier with increased folic acid transport mediates a novel mechanism of antifolate resistance. J. Biol. Chem., 273: 30189-30198, 1998.
6. Roy, K., Tolner, B., Chiao, J., and Sirotnak, F. A single amino acid difference within the folate transporter encoded by the murine RFC-1 gene selectively alters its interaction with folate analogues. J. Biol. Chem., 273: 2526-2531, 1998.
7. Roy, K., Egan, M., Sirlin, S., and Sirotnak, F. Posttranscriptionally mediated decreases in folylpolyglutamate synthetase gene expression in some folate analogue-resistant variants of the L1210 cell. J. Biol. Chem., 272: 6903-6908, 1997.
8. Rhee, M. S., Wang, Y., Nair, M. G., and Galivan, J. Acquisition of resistance to antifolates caused by enhanced γ-glutamyl hydrolase activity. Cancer Res., 53: 2227-2230, 1993.
9. Alt, F. W., Kellems, R. E., Bertino, J. R., and Schimke, R. T. Selective multiplication of dihydrofolate reductase genes in methotrexate resistant variants of cultured murine cells. J. Biol. Chem., 253: 1357-1370, 1978.
10. RIH. J. Biol. Chem., 265: 8317-8321, 1990.
11. Yu, M., and Melera, P. Allelic variation in the dihydrofolate reductase gene at amino acid position 95 contributes to antifolate resistance in Chinese hamster cells. Cancer Res., 53: 6031-6035, 1993.
12. Srimatkandada, S., Schweitzer, B. I., Moroson, B. A., Dube, S., and Bertino, J. R. Amplification of a polymorphic dihydrofolate reductase gene expressing an enzyme with decreased binding to methotrexate in a human colon carcinoma cell line, HCT-8R4, resistant to this drug. J. Biol. Chem., 264: 3524-3528, 1989.
13. Sirotnak, F., and O'Leary, D. The issues of transport multiplicity and energetics pertaining to methotrexate efflux in L1210 cells addressed by an analysis of cis and trans effects of inhibitors. Cancer Res., 51: 1412-1417, 1991.
14. Schlemmer, S., and Sirotnak, F. Energy-dependent efflux of methotrexate in L1210 leukemia cells. J. Biol. Chem., 267: 14746-14752, 1992.
15. Schlemmer, S., and Sirotnak, F. Retentiveness of methotrexate polyglutamates in cultured L1210 cells. Biochem. Pharmacol., 45: 1261-1266, 1993.
16. Schlemmer, S., and Sirotnak, F. Structural preferences among folate compounds and their analogues for ATPase-mediated efflux by inside-out plasma membrane vesicles derived from L1210 cells. Biochem. Pharmacol., 49: 1427-1433, 1995.
17. Saxena, M., and Henderson, G. B. Identification of efflux systems for large anionic conjugates as the mediators of methotrexate efflux in L1210 cells. Biochem. Pharmacol., 51: 975-982, 1996.
18. Jansen, G., Barr, H., Kathmenn, I., Bunni, M., Priest, D., Noordhuis, P., Peters, G., and Assaraf, Y. Multiple mechanisms of resistance to polyglutamatable and lipophilic antifolales in mammalian cells: role of increased folylpolyglutamylation, expanded folate pools, and intralysosomal drug sequestration. Mol. Pharm., 55: 761-769, 1999.
19. Higgins, C. F. ABC transporters: from microorganisms to man. Annu. Rev. Cell Biol., 8: 67-113, 1992.
20. Allikmets, R., Gerrard, B., Hutchinson, A., and Dean, M. Characterization of the human ABC superfamily: isolation and mapping of 21 new genes using the expressed sequence tags database. Hum. Mol. Genet., 5: 1649-1655, 1996.
21. Juliano, R. L., and Ling, V. A surface glycoprotein modulating drug permeability in Chinese hamster cell mutants. Biochim. Biophys. Acta. 455: 152-162, 1976.
22. Norris, M. D., De Graaf, D., Haber, M., Kavallaris, M., Madafiglio, J., Gilbert, J., Kwan, E., Stewart, B., Mechetner, E. B., Gudkov, A. V., and Roninson, I. B. Involvement of MDR1 P-glycoprotein in multifactorial resistance to methotrexate. Int. J. Cancer, 65: 613-619, 1996.
23. Bosch, I., and Croop, J. P-glycoprotein multidrug resistance and cancer. Biochim. Biophys. Acta. 1288: F37-F54, 1996.
24. Cole, S. P. C., Bhardwaj, G., Gerlach, J. H., Mackie, J. E., Grant, C. E., Almquist, K. C., Stewart, A. J., Kurz, E. U., Duncan, A. M. V., and Deeley, R. G. Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science (Washington DC), 258: 1650-1654, 1992.
25. Keppler, D., Leier, I., and Jedlitschky, G. Transport of glutathione conjugates and glucuronides by the multidrug resistance proteins MRP1 and MRP2. J. Biol. Chem., 378: 787-791, 1997.
26. Cole, S. P. C., Sparks, K. E., Fraser, K., Loe, D. W., Grant, C. E., Wilson, G. M., and Deeley, R. G. Pharmacological characterization of multidrug resistant MRP-transfected human tumor cells. Cancer Res., 54: 5902-5910, 1994.
27. Hirohashi, T., Suzuki, H., and Sugiyama, Y. Characterization of the transport properties of cloned rat multidrug resistance-associated protein 3 (MRP3). J. Biol. Chem., 274: 15181-15185, 1999.
28. Hooijberg, J. H., Broxterman, H. J., Kool, M., Assaraf, Y. G., Peters, G., Noordhuis, P., Scheper, R. J., Borst, P., Pinedo, H. M., and Jansen, G. Antifolate resistance mediated by the multidrug resistance proteins MRP1 and MRP2. Cancer Res., 59: 2532-2535, 1999.
29. Yang, C.-H. J., Horton, J. K., Cowan, K. H., and Schneider, E. Cross-resistance to camptothecin analogues in a mitoxantrone-resistant human breast carcinoma cell line is not due to DNA topoisomerase 1 alterations. Cancer Res., 55: 4004-4009, 1995.
30. Ross, D. D., Yang, W., Abruzzo, L. V., Dalton, W. S., Schneider, E., Lage, H., Dietel, M., Greenberger, L., Cole, S. P. C., and Doyle, L. A. Atypical multidrug resistance: breast cancer resistance protein messenger RNA expression in mitoxantrone-selected cell lines. J. Natl. Cancer Inst., 91: 429-433, 1999.
31. Doyle, L. A., Yang, W., Abruzzo, L. V., Krogmann, T., Gao, Y., Rishi, A. K., and Ross, D. D. A multidrug resistance transporter from human MCF-7 breast cancer cells. Proc. Natl. Acad. Sci. USA, 95: 15665-15670, 1998.
32. Miyake, K., Mickley, L., Litman, T., Zhan, Z., Robey, R., Cristensen, B., Brangi, M., Greenberger, L., Dean, M., Fojo, T., and Bates, S. E. Molecular cloning of cDNAs which are highly overexpressed in mitoxantrone-resistant cells: demonstration of homology to ABC transport genes. Cancer Res., 59: 8-13, 1999.
33. Allikmets, R., Schriml, L., Hutchinson, A., Romano-Spica, V., and Dean, M. A human placenta-specific ATP-binding cassette gene (ABCP) on chromosome 4q22 that is involved in multidrug resistance. Cancer Res., 58: 5337-5339, 1998.
34. Nakagawa, M., Schneider, E., Dixon, K. H., Horton, J., Kelley, K., Morrow, C., and Cowan, K. H. Reduced intracellular drug accumulation in the absence of P-glycoprotein (mdr1) overexpression in mitoxantrone-resistant MCF-7 breast cancer cells. Cancer Res., 52: 6175-6181, 1992.
35. Cowan, K. H., Goldsmith, M. E., Levine, R. M., Aitken, S. C. Douglass, E., Clendeninn, N., Nienhuis, A. W., and Lippman, M. E. Dihydrofolate reductase gene amplification and possible rearrangement in estrogen-responsive methotrexate-resistant human breast cancer cells. J. Biol. Chem., 257: 15079-15086, 1982.
36. Schneider, E., Horton, J. K., Yang, C.-H., Nakagawa, M., and Cowan, K. H. Multidrug resistance-associated protein gene overexpression and reduced drug sensitivity of topoisomerase II in a human breast carcinoma MCF7 cell line selected for etoposide resistance. Cancer Res., 54: 152-158, 1994.
37. Skehan, P., Storeng, R., Scudiero, D., Monks, A., McMahon, J., Vistica, D., Warren, J. T., Bokesch, H., Kenney, S., and Boyd, M. R. New colorimetric cytotoxicity assay for anticancer-drug screening. J. Natl. Cancer Inst., 82: 1107-1112, 1990.
38. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72: 248-254, 1976.
39. Rhee, M. S., Lindau-Shepard, B., Chave, K. J., Galivan, J., and Ryan, T. J. Characterization of human cellular γ-glutamyl hydrolase. Mol. Pharmacol., 53: 1040-1046, 1998.
40. Moscow, J. A., Gong, M., He, R., Sgagias, M. K., Dixon, K. H., Anzick, S. L., Meltzer, P. S., and Cowan, K. H. Isolation of a gene encoding a human reduced folate carrier (RFC1) and analysis of its expression in transport-deficient, methotrexate-resistant human breast cancer cells. Cancer Res., 55: 3790-3794, 1995.
41. McGuire, J. J., and Russell, C. A. Folylpolyglutamate synthetase expression in antifolate-sensitive and -resistant human cell lines. Oncol. Res., 10: 193-200, 1998.
42. O'Connor, B. M., Rotundo, R. F., Nimec, Z., McGuire, J. J., and Galivan, J. Secretion of γ-glutamyl hydrolase in vitro, Cancer Res., 51: 3874-3881, 1991.
43. Mathews, C. K., and Huennekens, F. M. Further studies on dihydrofolate reductase. J. Biol. Chem., 238: 3436-3442, 1963.
44. McGuire, J. J., Hsieh, P., Coward, J. K., and Bertino, J. R. In vitro methotrexate polyglutamate synthesis by rat liver folylpolyglutamate synthetase and inhibition by bromosulfothalein. In: I. D. Goldman, B. A. Chabner, and J. R. Bertino (eds.), Folyl and Antifolylpolyglutamates, pp. 199-214. New York: Plenum Publishing, 1983.
45. Gifford, A., Kavallaris, M., Madafiglio, J., Matherly, L., Stewart, B., Haber, M., and Norris, M. P-glycoprotein-mediated methotrexate resistance in CCRF-CEM sublines deficient in methotrexate accumulation due to a point mutation in the reduced folate carrier gene. Intl. J. Cancer, 78: 176-181, 1998.
46. Kool, M., van der Linden, M., de Haas, M., Scheffer, G. L., de Vree, J. M. L., Smith, A. J., Jansen, G., Peters, G. J., Ponne, N., Scheper, R. J., Elferink, R. P., Baas, F., and Borst, P. MRP3, an organic anion transporter able to transport anti-cancer drugs. Proc. Natl. Acad. Sci. USA, 96: 6914-6919, 1999.
47. Masuda, M., I'izuka, Y., Yamazake, M., Nishigaki, R., Kato, Y., Ni'inuma, K., Suzuki, H., and Sugiyama, Y. Methotrexate is excreted into the bile by canicular multispecific organic anion transporter in rats. Cancer Res., 57: 3506-3510, 1997.
48. Bakos, E., Evers, R., Sinko, E., Varadi, A., Borst, P., and Sarkadi, B. Interactions of the human multidrug resistance proteins MRP1 and MRP2 with organic anions. Mol. Pharmacol., 57: 760-768, 2000.
49. Ohnuma, T., Lo, R. J., Scanlon, K. J., Kamen, B. A., Ohnoshi, T., Wolman, S. R., and Holland, J. F. Evolution of methotrexate resistance of human acute lymphoblastic leukemia cells in vitro. Cancer Res., 45: 1815-1822, 1985.
50. Moscow, J. A., Connolly, T., Myers, T. G., Cheng, C. C., Paull, K., and Cowan, K. H. Reduced folate carrier gene (RFC1) expression and anti-folate resistance in transfected and non-selected cell lines. Int. J. Cancer, 72: 184-190, 1997.
51. Haber, D. A., Beverly, S. M., Kiely, M. L., and Schimke, R. T. Properties of an altered dihydrofolate reductase encoded by amplified genes in cultured mouse fibroblasts. J. Biol. Chem., 256: 9501-9510, 1981.
52. Moscow, J. A., Johnston, P. G., Cole, D., Poplack, D. G., and Cowan, K. H. Characterization of cross-resistance to methotrexate in a human breast cancer cell line selected for resistance to melphalan. Biochem. Pharmacol., 49: 1069-1078, 1995.
53. Schneider, E., Cowan, K. H., Bader, H., Toomey, S., Schwartz, G. N., Karp, J. E., Burke, P. J., and Kaufmann, S. H. Increased expression of the multidrug resistance-associated protein gene in relapsed acute leukemia. Blood, 85: 186-193, 1995.
54. Schneider, E., Yamazaki, H., Sinha, B. K., and Cowan, K. H. Buthionine sulphoximine-mediated sensitization of etoposide-resistant human breast cancer MCF7 cells overexpressing the multidrug resistance-associated protein involves increased drug accumulation. Br. J. Cancer, 71: 738-743, 1995.
55. Dembo, M., Sirotnak, F. M., and Moccio, D. M. Effects of metabolic deprivation on methotrexate transport in L1210 leukemia cells: further evidence for separate influx and efflux systems with different energetic requirements. J. Membr. Biol., 78: 9-17, 1984.
56. de Graaf, D., Sharma, R., Mechetner, E., Schimke, R., and Roninson, I. P-glycoprotein confers methotrexate resistance in 3T6 cells with deficient carrier-mediated methotrexate uptake. Proc. Natl. Acad. Sci. USA, 93: 1238-1242, 1996.
57. van Triest, B., Pinedo, H. M., Telleman, F., van der Wilt, C. L., Jansen, G., and Peters, G. J. Cross-resistance to antifolates in multidrug resistant cell lines with P-glycoprotein or multidrug resistance protein expression. Biochem. Pharmacol., 53: 1855-1866, 1997.
58. Rocchi, E., Khodjakov, A., Volk, E. L., Yang, C. H., Litman, T., Bates, S. E., and Schneider, E. The product of the ABC half-transporter gene ABCG2 (BCRP/MXR/ ABCP) is expressed in the plasma membrane. Biochem. Biophys. Res. Commun., 27: 42-46, 2000.